Passive Acoustic Monitoring (PAM) provides the way to feature the status, presence and trends of species’ distribution in different landscapes, under different environmental conditions. The howler monkeys are known for investing a long time and energy in the vocal type known as roar, an important vocal type for intra- and inter-group dynamics. The aim of the present study was to evaluate the detection, distribution and vocal behavior of wild howler monkeys based on the PAM methodology due to the need of having a fast and effective method to evaluate this species’ population presence and status given the successive yellow fever outbreaks lethally affecting it. The study was carried out at Fontes do Ipiranga State Park, Southeastern São Paulo City, Brazil. The evaluation of howler monkeys roar vocal behavior’s temporal pattern was carried out by taking into consideration the number of roaring events counted based on time. Vocalization occurrences observed between stations were compared to express the roaring events on an hourly basis. In total, 1,531 hours of recordings were analyzed and it allowed detecting roars in all PAM stations. The number of roaring events ranged from 71 to 142 per station. The present study has shown the useful application of PAM to accurately detect the presence of howler monkey groups based on vocal behavior. Furthermore, this method helps assessing groups’ distribution and daily occurrence, besides giving tips about how they are distributed in the area based on their handling ability.
Research Article
Passive Acoustic Monitoring application to evaluate the vocal behavior of wild howler monkeys (Alouatta guariba clamitans)
https://doi.org/10.21203/rs.3.rs-2073696/v1
This work is licensed under a CC BY 4.0 License
Version 1
posted
You are reading this latest preprint version
Automated recording unit
Vocalizations
Primates
Long-distance acoustic communication
Passive Acoustic Monitoring (PAM) in combination to bioacoustics analysis of species’ vocal behavior has been effective for population detection and evaluation in comparison to traditional methodologies used to do so (Zwart et al. 2014). Such a methodological approach is based on species’ vocal behavior; therefore, understanding vocalizations’ “way and function” is essential to help developing better data collection and analysis methods.
Accordingly, Cerqueira and Aide (2016) stated that PAM provides the way to feature the status, presence and trends of species’ distribution in different landscapes, under different environmental conditions. Autonomous Recording Units (ARUs) are installed to register sound waves in the study site in typical PAM programs, based on previously established sampling window (in KHz). Therefore, acoustic monitoring is appropriate to capture data about the presence, occurrence and distribution of sound-producer species (Furnas and Callas 2015).
Long-distance acoustic communication regards the transmission and reception of signs that carry along important messages, such as territory properties, social status, partners’ attraction and species identity (Catchpole and Slater, 2003; Bradbury and Vehrencamp, 2011). Acoustic features of this vocal type show that most of them have long amplitude and low frequencies due to higher energy concentration (below 1.5 KHz). This feature accounts for the long-reach transmission phenomenon (Mitani & Stuht 1998).
Thus, howler monkeys (Alouatta spp.) are known for investing a long time and energy in the vocal type known as roar (Oliveira & Ades, 2004; da Cunha & Byrne, 2006). Studies have already suggested that roaring works to keep groups of different howler monkeys away from each other (Alouatta palliata, Baldwin & Baldwin, 1976; Alouatta seniculus, Sekulic, 1982; da Cunha & Byrne 2006; da Cunha and Jalles-Filho, 2007). However, other studies give additional functions to roaring, such as to evaluate the relative-fight skills of alien individuals (Alouatta fusca, Chiarello, 1995; Alouatta pigra, Kitchen, 2004), to defend female partners (Holzmann, 2006) or roaring associated with the availability of food resources (Alouatta pigra, Van Belle & Estrada, 2020). These functional features of roaring point towards the fact that its detection in a given location depends on the number of groups in it and on the availability of food and females.
According to the aforementioned information, we assume the importance of ‘roaring’ for intra- and inter-group dynamics, mainly as appropriate vocal type for howler monkey population and environmental context’s evaluations. The aim of the present study was to evaluate the detection, distribution and vocal behavior of wild howler monkeys based on the Passive Acoustic Monitoring methodology due to the need of having a fast and effective method to evaluate this species’ population presence and status given the successive yellow fever outbreaks lethally affecting it.
Study site
The current study was carried out at Fontes do Ipiranga State Park (PEFI), Southeastern São Paulo City, Brazil. PEFI’s total area covers 526 ha, and it is seen as an important Atlantic Forest remnant in São Paulo City (Gomes et al. 2003; Tanus et al. 2012). The area around PEFI is urbanized, and it fully isolates the park from other forest areas (Formenton-Silva and Rancura 2020). This park is split into four large Institutions: São Paulo Zoo Foundations (FPZSP), Botanic Institute (IBOT) USO Science and Technology Park (CIENTEC) and São Paulo Agriculture and Supply Secretariat. We selected BOT and CIENTEC areas for the present study (Figure 1).
Assessed species
Species Alouatta guariba clamitans (Cabrera, 1940) was selected for the study; this is a howler monkey species endemic to the Atlantic Forest and its distribution goes from Espírito Santo State to Rio Grande do Sul State (Mittermeier et al. 1982). Groups of A. g. clamitans range from 2 to 13 individuals and their reproduction is not seasonal; therefore, it can be observed all year long (Miranda & Passos, 2005). Estimates show that the mean number of howler monkeys at PEFI reaches 549 individuals and that each group may present life area of 4.55ha (Benedicto 2015).
Data collection
AudioMoth’s (Open Acoustics Devices) adjusted to installation in forest environment was used for passive recording purposes by taking into consideration humidity and exposure to other climate elements. Recording time configurations were set based on previous studies about howler monkey’s vocal activity evaluation. Thus, option was made to conduct the recordings between 05:00 am and 05:00 pm (local time) (da Cunha and Jalles-Filho 2007; Oliveira and Ades 2010). Recordings in each area are detailed in Table 1.
Table 1. Summary of recordings conducted in the year 2021.
|
Area |
Stations |
Dates of record |
Sunrise/sunset average (UTC) |
Total hours of records |
|
IBOT |
Pod01 |
04 November to 04 December |
07:40 / 19:59 |
250 |
|
Pod02 |
252 |
|||
|
Pod03 |
257 |
|||
|
CIENTEC |
Pod04 |
256 |
||
|
Pod05 |
259 |
|||
|
Pod06 |
257 |
Recordings were carried out from November to December 2021. Three recording machines were installed in each location (IBOT and CENTEC) and it totaled 6 recording stations. The recording machines were equipped with omnidirectional microphone adapted to record at sampling rate of 8 kHz; sounds were digitally recorded in wav format at 16 bits. Each recording machine was placed approximately 2-m above the ground.
Vocal behavior analysis
Software Raven Pro version 1.5 (Raven Pro: Interactive Sound Analysis Software, Ithaca, NY: The Cornell Lab of Ornithology) was used to analyze howler monkey’s vocal behavior. The selection of roaring events was carried out throughout the audio evaluation procedure by giving it an analysis window or “sampling window”.
Evaluation of howler monkeys roar vocal behavior’s temporal pattern was carried out by taking into consideration the number of roaring events counted based on time (05:00 am to 05:00 pm, local time). Vocalization occurrences observed between stations were compared to express the roaring events on an hourly basis. Analysis of variance applied to one factor (one-way ANOVA) was performed to compare roars distribution among stations; it was followed by post-hoc Tukey test (DMS) based on groups’ percentiles.
In total, 1,531 hours of recordings were analyzed and it allowed detecting roars in all PAM stations (pod01 to pod06). The number of roaring events ranged from 71 to 142 per station (Figure 3). The highest level of roaring presence was observed in pod01 (n=142; X=6.92; sd=5.50; 21 days), at IBOT. On the other hand, pod6 (CIENTEC) showed the lowest levels of roaring events (n=71; X=4.23; sd=3.90; 21 days). Roaring events were more significant at 09:00 am (n=667), in all recording stations (Figure 4).
According to the analysis, there is no difference in the distribution of roar occurrences among all stations (one-way ANOVA, F=0.72; p=0.61) (Table 2).
Table 2. Summary of post hoc Tukey test (DMS) results comparing the distribution of roar activity in all PAM stations.
Therefore, there are two possibilities for such a result: the first one is based on the premise that we have detected the same groups in stations IBOT and CIENTEC, and it has led to equal distributions; the second possibility is based on the species’ vocal behavior pattern, which is expected to show a broader vocal activity in the morning and at early afternoon; thus, groups detected in each station have shown the same temporal pattern of vocal behavior.
Results in the present study provide a methodological approach to measure the presence and distribution of A. g. clamitans based on using the Passive Acoustic Monitoring to assess this species’ vocal behavior. Roars were detected in all PAM stations and it suggested the presence of groups either in IBOT or in CIENTEC. Granados and Schuchmann (2021) assessed the Alouatta caraya population in the Brazilian Pantanal through PAM and observed vocal activity peak between 05:00 and 06:00 am (Brasília time); this finding is in compliance with the study we have carried out with A. g. clamitans at PEFI.
Accordingly, results in the current study have reinforced previous knowledge about the vocal activity of individuals belonging to genus Alouatta sp. (Whitehead 1995; da Cunha et al. 2015; Van Belle et al. 2013). This is the starting point to elaborate wild group monitoring programs focused on vocal activity time peaks - in our case, from 05:00 am to 11:00 am (local time).
A. g. clamitans population at PEFI has been facing a series of impacts from urbanization, such as electrocution, being run over and injuries from falling onto asphalt (Monticelli 2019). Previous studies carried out with this population have shown that groups were featured as harems leaded by an alpha male who seeks to centralize access to reproduction with females in the group (Monticelli 2019); in other words, it shows the insular profile of this population’s life context, in addition to the likely shortage of resources, a fact that can lead to higher rates of territorial and agonistic behavior. Thus, based on the present results, A. g. clamitans at PEFI have emitted roars, territorial and agonistic function vocalizations, on a daily basis, during the recording times; there were days when all PAM stations showed roars at the same time. This finding evidences traces that the PEFI area may not support the A. g. clamitans population due to the amount of resources available in it. The study conducted by Monticelli (2019) with groups of A. g. clamitans at PEFI provided evidences that males’ territorial behavior generated intra-specific conflicts. The aforementioned author believes that such a fact results from dispute for resources. Actually, the life area of Alouatta sp. is closely associated with groups’ ability to enter fragmented environments (Crockett, 1998; Bicca-Marques, 2003). In order to do so, emitting roars is the main behavior expected for this life context.
Two groups of A. g. clamitans from different areas at PEFI were followed-up for 12 months; their life area was estimated in 3.5 and 5.6 ha, respectively (Benedicto et al. 2015). Both groups were located in the IBOT area, the group occupying the largest area was living in the largest preservation and connectivity zone at PEFI. Therefore, groups are found in the lines of smallest life areas reported for the species. Thus, assumingly, the smallest life areas likely derive from the high population density suggested for the study site (Benedicto et al. 2015), a fact that can account for the highest possibility of interaction among different groups.
According to Granados and Schuchmann (2021), our study presents few limitations related to control group size and individuals’ distancing from PAM stations. Findings in our acoustic screening suggested that howler monkey populations at PEFI were not affected by yellow fever, as well as other populations of this species in São Paulo State, Brazil. This species is endangered based on the list of endangered animals of São Paulo State (São Paulo 2018); it is categorized as vulnerable species in other evaluation lists (MMA 2018) and globally classified as not concerning species (IUCN 2008). Nevertheless, despite such different evaluations, there is consensus that the A. g. clamitans population tends to decrease throughout its occurrence area. Therefore, research efforts and investment aimed at evaluating and monitoring the A. g. clamitans population are needed, mainly in São Paulo State.
The present study has shown the useful application of passive acoustic monitoring to accurately detect the presence of howler monkey groups based on vocal behavior. Furthermore, this method helps assessing groups’ distribution and daily occurrence, besides giving tips about how they are distributed in the area based on their handling ability.
The process to track space-temporal changes in howler monkey’s vocal activity can still be used to inform conservation priorities, to identify main resources, as well as threats to species A. g. clamitans. Finally, using autonomous-sound recording machines combined to other methods (among them, monitoring the behavior of this species in situ, in potential locations for long-term monitoring) can be a promising method for further studies aimed at surveilling primate groups.
This work was supported by FAPESP (São Paulo Research Foundation) (Grant numbers 19/20590-3). Author Bruna Campos Paula has received research support from CNPQ (National Council for Scientific and Technological Development) (Doctorate Scholarship).
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Author contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Bruna Campos Paula, Adriano Pinter and Linilson Padovese. The first draft of the manuscript was written by Bruna Campos Paula and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
- Baldwin JD, Baldwin JI (1976) Vocalizations of howler monkeys (Alouatta palliata) in southwestern Panama. Folia Primatol., 26(2), 81-108.
- Benedicto DM (2015) Área de vida, padrão de atividade, dieta e dispersão de sementes por Alouatta clamitans (Cabrera, 1940) em um fragmento urbano de Mata Atlântica da cidade de São Paulo. Dissertation, Universidade Federal de São Carlos.
- Bicca-Marques JC (2003) How do Howler Monkeys Cope with Habitat Fragmentation?. In: Marsh, LK (eds) Primates in Fragments, Springer, Boston, MA.
- Bradbury JW, Vehrencamp SL (2011) Principles of animal communication. Oxford University.
- Campos‐Cerqueira M, Aide MT (2016) Improving distribution data of threatened species by combining acoustic monitoring and occupancy modelling. Methods Ecol Evol 11: 1340-1348.
- Catchpole CK., Slater PJB (2003) Bird song: biological themes and variations. Cambridge university press.
- Chiarello, AG (1995) Role of loud calls in brown howlers, Alouatta fusca. Am J Primatol 36: 213-222.
- Crockett CM (1998) Conservation biology of the genus Alouatta, bit. J Primatol 19: 549–578.
- da Cunha RGT, Byrne RW (2006) Roars of black howler monkeys (Alouatta caraya): evidence for a function in inter-group spacing. Behaviour 143: 1169–1199.
- Da Cunha RGT, Jalles-FilhoE. (2007) The roaring of southern brown howler monkeys (Alouatta guariba clamitans) as a mechanism of active defence of borders. Folia Primatol 78: 259–271.
- Furnas BJ, Callas RL (2015) Using automated recorders and occupancy models to monitor common forest birds across a large geographic region. J Wildl Manage 79: 325–337.
- Gomes EPC, Mantovani W, Kageyama PY (2003) Mortality and recruitment of trees in a secondary montane rain forest in southeastern Brazil. Braz J Biol 63: 47–60.
- Holzmann I (2006) Vocal behaviour of Alouatta guariba and Alouatta caraya living in sympatry in El Piñalito Provincial Park in Misiones, Argentina. Rufford Small Grant Annual Report.
- Kitchen DM (2004) Alpha male black howler monkey responses to loud calls: effect of numeric odds, male companion behaviour and reproductive investment. Anim Behav 67: 125–139.
- Miranda J, Passos FC (2005) Composição e dinâmica de grupos de Alouatta guariba clamitans Cabrera (Primates, Atelidae) em Floresta Ombrófila Mista no estado do Paraná, Brasil. Rev Bras Zool 22: 99–106.
- Mitani JC, Stuht J (1998) The evolution of nonhuman primate loud calls: acoustic adaptation for long-distance transmission. Primates 39: 171–182.
- Mittermeier RA, Coimbra-Filho AF, Constable ID, Rylands AB, Valle C (1982) Conservation of primates in the Atlantic forest region of eastern Brazil. Int Zoo Yearb 22: 2–17.
- Monticelli C (2019) Diversidade genética de uma população isolada de bugio-ruivo (Alouatta guariba clamitans) (Cabrera 1940) no Parque Estadual das Fontes do Ipiranga, São Paulo–SP. Dissertation, Universidade Federal de São Carlos.
- Oliveira DA, Ades C (2004) Long-distance calls in Neotropical primates. An Acad Bras Ciênc 76: 393–398.
- Pérez‐Granados C, Schuchmann KL (2021) Passive acoustic monitoring of the diel and annual vocal behavior of the Black and Gold Howler Monkey. Am J Primatol 83: e23241.
- Silva-Lehmkuhl AMD, Lehmkuhl EA, Oliveira SAD, Morais KSD, Bicudo DC, Bicudo CEDM (2020) Criptógamos do Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Hoehnea 47.
- Tanus MR, Pastore M, Bianchini RS, Gomes EPC (2012) Estrutura e composição de um trecho de mata atlântica no Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Hoehnea 39: 157-168.
- Van Belle S, Estrada A (2020) The influence of loud calls on intergroup spacing mechanism in black howler monkeys (Alouatta pigra). Int J Primatol 41: 265–286.
- Zwart MC, Baker A, McGowan PJ, Whittingham MJ (2014) The use of automated bioacoustic recorders to replace human wildlife surveys: an example using nightjars. PloS one 9: e102770.
No competing interests reported.